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GENETICS AND MOLECULAR BIOLOGY

Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons

Silvia G. Acinas, Luisa A. Marcelino, Vanja Klepac-Ceraj, Martin F. Polz
Silvia G. Acinas
Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
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Luisa A. Marcelino
Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
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Vanja Klepac-Ceraj
Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
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Martin F. Polz
Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
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  • For correspondence: mpolz@mit.edu
DOI: 10.1128/JB.186.9.2629-2635.2004
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  • FIG. 1.
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    FIG. 1.

    Distribution of different rrn operon numbers among bacterial (gray bars) and archaeal (black bars) isolates. Data were obtained from complete genome sequences from the NCBI and TIGR genome databases, the rrndb database, and the literature.

  • FIG. 2.
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    FIG. 2.

    Numbers (bars) and percentages of the total (line) of genomes with all identical 16S rRNA sequences among operons. Data were retrieved from the NCBI and TIGR genome databases and the rrndb database.

  • FIG. 3.
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    FIG. 3.

    Secondary structure model of the helices that differ in length between operons in Thermoanaerobacter tengcongensis. Nucleotide positions 444 to 490 (A) and 1,447 to 1,456 (B) are given according to Escherichia coli reference numbering.

Tables

  • Figures
  • TABLE 1.

    Number of operons, heterogeneity and redundancy of 16S rRNA genes within bacterial and archaeal genomes with multiple operonsa

    Domain or microorganismPhylogenetic affiliationNo. of operonsNo. of identical operonsbNo. of different ribotypescNucleotide divergence (% 16S)dNo. of poly- morph- ismseSource or referencef
    Bacteria (76 genomes)
        Aquifex aeolicus VF5 Aquificales 22100rrndb
        Chlorobium tepidum TLS Chlorobiales 22100This paper
        Synechocystis sp. PCC 6803Cyanobacteria22100This paper
        Treponema pallidum ATCC 25870 Spirochaetales 22100rrndb
        Leptospira interrogans serovar Lai 56601 Spirochaetales 22100This paper
        Caulobacter crecentus CB15Alpha proteobacteria22100This paper
        Xanthomonas axonopodis pv. citri 306Gamma proteobacteria22100This paper
        Xylella fastidiosa 9a5cGamma proteobacteria22100rrndb
        Xanthomonas campestris ATCC 33913Gamma proteobacteria22100This paper
        Helicobacter pylori 26695Epsilon proteobacteria22100rrndb
        Helicobacter pylori J99Epsilon proteobacteria202NDND27
        Ureaplasma urealyticum serovar 3 Mycoplasmatales 2020.071rrndb
        Mycobacterium celatum Actinomycetales 202ND4/534
        Mycobacterium strain “X" Actinomycetales 2021.201830
        Desulfotomaculum kuznestovii Clostridales 2028.3ND40
        Chlamydia trachomatis Chlamydiae2210027
        Geobacter sulfurreducens Delta proteobacteria20/21/20/0.20/3This paper
        Deincoccus radiodurans ATCC 13939 Deinococcales 3220.132rrndb
        Rhodobacter sphaeroides Alpha proteobacteria3310010
        Brucella suis 1330, biovar 1Alpha proteobacteria33100This paper
        Brucella melitensis 16MAlpha proteobacteria33100This paper
        Sinorhizobium meliloti Alpha proteobacteria33100This paper
        Ralstonia solanacearum Beta proteobacteria33100This paper
        Campylobacter jenuni ATCC 700819Epsilon proteobacteria33100rrndb
        Nostoc sp. PCC 7120Cyanobacteria4320.071This paper
        Agrobacterium tumefaciens C58Alpha proteobacteria44100This paper
        Neisseria meningitidis MC58Alpha proteobacteria44100rrndb
        Pseudomonas aeruginosa PAO1Gamma proteobacteria42 + 220.071This paper
        Enterococcus faecalis V583 Firmicutes 43 + 120.071This paper
        Streptococcus pneumoniae R6 Firmicutes 44100This paper
        Streptococcus pneumoniae TIGR4 Firmicutes 44100This paper
        Thermobispora bispora R51 Actinomycetales 4046.49841
        Thermoanaerobacter tengcongensis Thermoanaerobacteriales 4046.5/11.699/188This paper
        Pseudomonas syringae pv tomato DC3000Gamma proteobacteria55100This paper
        Fusobacterium nucleatum subsp. nucleatum Fusobacteria52 + 1 + 1 + 140.203This paper
        Corynebacterium efficiens YS-314 Actinomycetales 54 + 120.21/0.423/6This paper
        Staphylococcus epidermidis ATCC 12228 Firmicutes 5050.8413This paper
        Staphylococcus aureus N315 Firmicutes 52 + 1 + 1 + 140.254This paper
        Staphylococcus aureus Mu50 Firmicutes 5050.386This paper
        Lactobacillus plantarum WCFS1 Firmicutes 52 + 2 + 130.132This paper
        Streptococcus mutans UA159 Firmicutes 53 + 220.193This paper
        Streptococcus pyogenes SSI-1 Firmicutes 55100This paper
        Clostridium tetani E88 Clostridiales 52 + 1 + 1 + 140.396This paper
        Desulfovibrio vulgaris Delta proteobacteria52 + 1 + 1 + 140.264This paper
        Bacteroides thetaiotaomicron VPI-5482 Bacteroidales 52 + 2 + 131.23/1.317/18This paper
        Haemophilus influenzae Rd (ATCC 51907)Gamma proteobacteria66100rrndb
        Yersina pestis CO92Gamma proteobacteria62 + 1 + 1 + 1 + 150.274This paper
        Corynebacterium glutamicum ATCC 13032 Actinomycetales 62 + 1 + 1 + 1 + 150.33/0.396This paper
        Thermomonospora chromogena Actinomycetales 6066ND43
        Staphylococcus aureus MW2 Firmicutes 63 + 1 + 1 + 140.325This paper
        Listeria monocytogenes EGD-e Firmicutes 62 + 2 + 1 + 140.325This paper
        Listeria innocua Clip 11262 Firmicutes 65 + 120.254This paper
        Lactococcus lactis subsp. lactis Firmicutes 65 + 120.061This paper
        Streptococcus pyogenes MGAS315 Firmicutes 66100This paper
        Streptococcus pyogenes M1 GAS (SF370) Firmicutes 63 + 2 + 130.075/0.151/2This paper
        Streptococcus pyogenes MGAS8232 Firmicutes 66100This paper
        Pseudomonas putida KT2440Gamma proteobacteria72 + 2 + 2 + 140.193This paper
        Shigella flexneri 2a 301Gamma proteobacteria74 + 2 + 130.51/0.588/9This paper
        Escherichia coli K-12Gamma proteobacteria73 + 1 + 1 + 1 + 151.23/1.3618/21This paper
        Escherichia coli EDL933 (O157:H7)Gamma proteobacteria72 + 1 + 1 + 1 + 1 + 160.45/0.977/15This paper
        Escherichia coli Sakai (O157:H7)Gamma proteobacteria73 + 2 + 1 + 140.45/0.587/9This paper
        Escherichia coli ATCC 10798Gamma proteobacteria73 + 1 + 1 + 1 + 151.2319rrndb
        Salmonella entercia serovar Typhimurium LT2Gamma proteobacteria73 + 1 + 1 + 1 + 150.64/0.589/10This paper
        Salmonella enterica subs P. enterica serovar TyphiGamma proteobacteria73 + 2 + 1 + 140.13/0.192/3This paper
        Salmonella enterica subs P. enterica serovar Typhi Ty2Gamma proteobacteria73 + 3 + 130.13/0.192/3This paper
        Yersina pestis KIM10+Gamma proteobacteria75 + 220.061This paper
        Oceanobacillus iheyensis HTE831 Firmicutes 73 + 1 + 1 + 1 + 150.96/1.0215/16This paper
        Streptococcus agalactiae NEM316 Firmicutes 76 + 120.071This paper
        Streptococcus agalactiae 2603 V/R Firmicutes 77100This paper
        Vibrio cholerae El Tor N16961Gamma proteobacteria8080.91/1.0412/14This paper
        Shewanella oneidensis MR-1Gamma proteobacteria94 + 3 + 1 + 140.325This paper
        Bacillus subtilis 168 Firmicutes 100101.48/2.1823/34This paper
        Clostridium perfringens 13 Clostridiales 100100.93/1.1814/1837; this paper
        Vibrio parahaemolyticus (RIMB22106633)Gamma proteobacteria112 + 2 + 2 + 1 + 1 + 1 + 1 + 180.619This paper
        Clostridium acetobutylicum Clostridiales 117 + 1 + 1 + 1 +150.26/0.924/14This paper
        Bacillus cereus ATCC 14579 Firmicutes 137 + 1 + 1 + 1 + 1 + 1 + 170.467This paper
    Archaea (5 genomes)
        Methanocaldococcus jannaschii Methanococcales (Euryarchaeota)2020.07/0.271/4rrndb; this paper
        Methanothermobacter thermoauto- trophicus Methanobacteriales (Euryarchaeota)2020.142rrndb
        Haloarcula marismortui Halobacteriales (Euryarchaeota)20257428
        Methanosarcina acetivorans C2A Methanosarcinales (Euryarchaeota)32 + 120.071This paper
        Methanosarcina mazei Goe1 Methanosarcinales (Euryarchaeota)33100This paper
    • ↵ a Data were obtained from the NCBI (www.ncbi.nlm.nih.gov/PMGifs/Genomes/micr.html ) and TIGR (www.tigr.org/tdb/mdbcomplete.html ) genome databases, the rrndb (http://rrndb.cme.msu.edu ) (22), and multiple literature sources.

    • ↵ b Different numbers indicate identical 16S rRNA gene sequences in genomes with multiple operons.

    • ↵ c Ribotypes are defined as identical 16S rRNA sequences.

    • ↵ d Divergence is represented by pairwise distances calculated from alignments of all 16S rRNA sequences for each genome. Single values indicate that there are no insertions or deletions (I/D). When two values are given, left values represent no I/D and right values are with I/D.

    • e The numbers of polymorphisms represent the cumulative numbers of sequence positions in which the aligned sequences differed. Single values indicate that there are no insertions or deletions (I/D). When two values are given, left values represent no I/D and right values are with I/D.

    • ↵ f ND, not determined. Analyses were performed on alignments generated for this paper unless other sources are listed.

  • TABLE 2.

    Strains of the same bacterial species with different numbers of rrn operonsa

    Microorganism namePhylogenetic affiliationNo. of rrn operon copies
    Borrelia burgdorferi Spirochaetales 1 and 2
    Chlamydia trachomatis Chlamydiae 1 and 2
    Rhodococcus fascians Actinomycetales 4 and 5
    Rhodopseudomonas palustris Alpha proteobacteria1 and 2
    Bradyrhizobium japonicum Alpha proteobacteria1 and 2
    Vibrio parahaemolyticus Gamma proteobacteria9 and 11
    Vibrio cholerae Gamma proteobacteria7, 8, and 9
    Pasteurella multocida Gamma proteobacteria5 and 6
    Yersinia pestis Gamma proteobacteria6 and 7
    Bacillus subtilis Firmicutes 9 and 10
    Bacillus anthracis Firmicutes 10 and 11
    Bacillus cereus Firmicutes 9, 12, and 13
    Staphylococcus aureus Firmicutes 5 and 6
    Enterococcus faecium Firmicutes 5 and 6
    Streptococcus agalactiae Firmicutes 6 and 7
    Streptococcus pyogenes Firmicutes 5 and 6
    • ↵ a Data were obtained from the NCBI genome database (http://www.ncbi.nlm.nih.gov/PMGifs/Genomes/micr.html ), the rrndb (http://rrndb.cme.msu.edu ) (22), and the literature (18, 20).

  • TABLE 3.

    Range and averages of percentages of nucleotide divergence in bacterial 16S rRNA sequences within genomes with multiple rrn operonsa

    No. of rrn operonsNo. of sequencesRange of divergence (%) (−I/D)Average (%) (−I/D)Range of divergence (%) (+I/D)Average (%) (+I/D)
    2b 150-1.20.090-1.20.1
    370-0.130.0180-0.130.018
    4b 70-0.070.030-0.070.03
    5120-1.230.340-1.360.363
    6b 100-0.330.1620-0.390.176
    7130-1.230.3960-1.360.487
    820.910.911.041.04
    910.320.320.320.32
    1030.97-1.481.150.97-2.181.46
    1120.26-0.610.4350.61-0.920.765
    1210.330.330.330.33
    132NANANANA
    151NANANANA
    • ↵ a Data were obtained from the NCBI (www.ncbi.nlm.nih.gov/PMGifs/Genomes/micr.html ) and TIGR (www.tigr.org/tdb/mdb/mdbcomplete.html ) genome databases, the rrndb (http://rrndb.cme.msu.edu ) (22), and multiple literature sources. NA, no rrn operon sequences were available.

    • ↵ b Four cases of extreme divergence (sequences from microorganisms in which the percentage of nucleotide divergence was much higher than the average) were excluded from the calculation. These were Desulfotomaculum kuznestovii, with two rrn operons and an 8.3% difference, Thermobispora bispora R51 and Thermoanaerobacter tengcongensis, both with four rrn operons and 6.4 and 11.6% differences, respectively, and Thermonospora chromogena, with six rrn operons and 6% divergence.

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Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons
Silvia G. Acinas, Luisa A. Marcelino, Vanja Klepac-Ceraj, Martin F. Polz
Journal of Bacteriology Apr 2004, 186 (9) 2629-2635; DOI: 10.1128/JB.186.9.2629-2635.2004

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Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons
Silvia G. Acinas, Luisa A. Marcelino, Vanja Klepac-Ceraj, Martin F. Polz
Journal of Bacteriology Apr 2004, 186 (9) 2629-2635; DOI: 10.1128/JB.186.9.2629-2635.2004
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KEYWORDS

Genome, Archaeal
Genome, Bacterial
operon
RNA, Ribosomal, 16S

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